Phylotranscriptomic evidence for pervasive ancient hybridization among Old World salamanders

Rancilhac, Loïs; Irisarri, Iker; Angelini, Claudio; Arntzen, Jan W.; Babik, Wiesław; Bossuyt, Franky; Künzel, Sven; Lüddecke, Tim; Pasmans, Frank; Sanchez, Eugenia; Weisrock, David W.; Veith, Michael; Wielstra, Ben; Steinfartz, Sebastian; Hofreiter, Michael; Piégay, Hervé; Vences, Miguel

doi:10.1016/j.ympev.2020.106967

Cited by 23 publications

(13 citation statements)

References 91 publications

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“…The calculations were performed in codeml from PAML 4.9 ( Yang 2007 ). A comprehensive phylogeny of the Urodela ( Jetz and Pyron 2018 ), modified to include the most recent phylogeny of the Salamandridae ( Rancilhac et al 2021 ), was used as the phylogenetic tree in all the analyses except those of PSMB8 and PSMB9 . For these two genes, maximum likelihood trees under the General Time Reversible model of evolution were constructed with MEGA7 ( Kumar et al.…”

Section: Methodsmentioning

confidence: 99%

Molecular Evolution of Antigen-Processing Genes in Salamanders: Do They Coevolve withMHCClass I Genes?

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Dudek

Wielstra

et al. 2021

Genome Biology and Evolution

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Proteins encoded by Antigen Processing Genes (APGs) prepare antigens for presentation by the Major Histocompatibility Complex class I (MHC I) molecules. Coevolution between APGs and MHC I genes has been proposed as the ancestral gnathostome condition. The hypothesis predicts a single highly expressed MHC I gene and tight linkage between APGs and MHC I. In addition, APGs should evolve under positive selection, a consequence of the adaptive evolution in MHC I. The presence of multiple highly expressed MHC I genes in some teleosts, birds, and urodeles appears incompatible with the coevolution hypothesis. Here, we use urodele amphibians to test two key expectations derived from the coevolution hypothesis: i) the linkage between APGs and MHC I was studied in Lissotriton newts, and ii) the evidence for adaptive evolution in APGs was assessed using 42 urodele species comprising 21 genera from seven families. We demonstrated that five APGs (PSMB8, PSMB9, TAP1, TAP2 and TAPBP) are tightly linked (< 0.5 cM) to MHC I. Although all APGs showed some codons under episodic positive selection, we did not find a pervasive signal of positive selection expected under the coevolution hypothesis. Gene duplications, putative gene losses, and divergent allelic lineages detected in some APGs demonstrate considerable evolutionary dynamics of APGs in salamanders. Overall, our results indicate that if coevolution between APGs and MHC I occurred in urodeles, it would be more complex than envisaged in the original formulation of the hypothesis.

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Section: Methodsmentioning

confidence: 99%

Molecular Evolution of Antigen-Processing Genes in Salamanders: Do They Coevolve withMHCClass I Genes?

Palomar

Dudek

Wielstra

et al. 2021

Genome Biology and Evolution

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“…For geographical distribution of the (sub-)species of the genus Lissotriton (after Ianella et al, 2017;Wielstra et al, 2018) and sample localities see Figure S1. The phylogenetic relationships of the studied taxa are described by Pabijan et al (2017) and Rancilhac et al (2020).…”

Section: Materials S and Me Thodsmentioning

confidence: 99%

Variation in vertebrae shape across small‐bodied newts reveals functional and developmental constraints acting upon the trunk region

et al. 2021

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The vertebral column forms the central axis of the vertebrate body and has a crucial role in body support and locomotion. It is composed of a number of repetitive, serially homologous skeletal elementsthe vertebrae. The homeobox (Hox) genes are known to be directly involved in somite and vertebrae formation and play a key role in the attainment of vertebral identity (Krumlauf, 1994;Mallo et al., 2010;Woltering, 2012). It has been proposed that different vertebral morphologies are governed by unique combinations of Hox genes expressed in the somites (Kessel & Gruss, 1991;Wellik, 2007) with the corollary that few Hox genes expression boundaries can be used as markers for regional differentiation of the axial skeleton (Böhmer et al., 2015;Burke et al., 1995;Narita & Kuratani, 2005). For example, the cervico-thoracic transition in amniotes is determined by Hox-5 and Hox-6 genes and the formation of the lumbo-sacral boundary is under control of the Hox-10 and Hox-11 genes (Wellik & Capecchi, 2003). Recent morphometric studies have provided new insight into presacral vertebral regionalization in amniotes (Head &

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“…Therefore, both recent and ancient gene flow might explain the high degree of topological incongruence within this clade. Evidence of ancient gene flow, dating back to early stages of lineage divergence, have been found in a growing number of studies based on genomic data ( Li et al 2016 ; Wen et al 2016 ; Zarza et al 2016 ; Meier et al 2017 ; Burbrink and Gehara 2018 ; Harris et al 2018 ; Thom et al 2018 ; Edelman et al 2019 ; MacGuigan and Near 2019 ; Pulido-Santacruz et al 2020 , Rancilhac et al 2021 ). Zhang et al (2019) suggested that the strong mito-nuclear discordance and topological conflicts within another clade of Phylloscopus species were due to “ghost introgression” from an extinct species.…”

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Most Genomic Loci Misrepresent the Phylogeny of an Avian Radiation Because of Ancient Gene Flow

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Phylogenetic trees based on genome-wide sequence data may not always represent the true evolutionary history for a variety of reasons. One process that can lead to incorrect reconstruction of species phylogenies is gene flow, especially if interspecific gene flow has affected large parts of the genome. We investigated phylogenetic relationships within a clade comprising eight species of passerine birds (Phylloscopidae, Phylloscopus, leaf warblers) using one de novo genome assembly and 78 resequenced genomes. On the basis of hypothesis-exclusion trials based on D-statistics, phylogenetic network analysis and demographic inference analysis, we identified ancient gene flow affecting large parts of the genome between one species and the ancestral lineage of a sister species pair. This ancient gene flow consistently caused erroneous reconstruction of the phylogeny when using large amounts of genome-wide sequence data. In contrast, the true relationships were captured when smaller parts of the genome were analyzed, showing that the “winner-takes-all democratic majority tree” is not necessarily the true species tree. Under this condition, smaller amounts of data may sometimes avoid the effects of gene flow due to stochastic sampling, as hidden reticulation histories are more likely to emerge from the use of larger datasets, especially whole-genome datasets. In addition, we also found that genomic regions affected by ancient gene flow generally exhibited higher genomic differentiation but a lower recombination rate and nucleotide diversity. Our study highlights the importance of considering reticulation in phylogenetic reconstructions in the genomic era.

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Phylotranscriptomic evidence for pervasive ancient hybridization among Old World salamanders

Cited by 23 publications

References 91 publications

Molecular Evolution of Antigen-Processing Genes in Salamanders: Do They Coevolve withMHCClass I Genes?

Molecular Evolution of Antigen-Processing Genes in Salamanders: Do They Coevolve withMHCClass I Genes?

Variation in vertebrae shape across small‐bodied newts reveals functional and developmental constraints acting upon the trunk region

Most Genomic Loci Misrepresent the Phylogeny of an Avian Radiation Because of Ancient Gene Flow

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